Wing patterning genes and coevolution of Müllerian mimicry inHeliconiusbutterflies: Support from phylogeography, cophylogeny, and divergence times

Examples of long-term coevolution are rare among free-living organisms. Müllerian mimicry in Heliconius butterflies had been suggested as a key example of coevolution by early genetic studies. However, research over the last two decades has been dominated by the idea that the best-studied comimics, H. erato and H. melpomene, did not coevolve at all. Recently sequenced genes associated with wing color pattern phenotype offer a new opportunity to resolve this controversy. Here, we test the hypothesis of coevolution between H. erato and H. melpomene using Bayesian multilocus analysis of five color pattern genes and five neutral genetic markers. We first explore the extent of phylogenetic agreement versus conflict between the different genes. Coevolution is then tested against three aspects of the mimicry diversifications: phylogenetic branching patterns, divergence times, and, for the first time, phylogeographic histories. We show that all three lines of evidence are compatible with strict coevolution of the diverse mimicry wing patterns, contrary to some recent suggestions. Instead, these findings tally with a coevolutionary diversification driven primarily by the ecological force of Müllerian mimicry

Impacts of speciation and extinction measured by an evolutionary decay clock

The hypothesis that destructive mass extinctions enable creative evolutionary radiations (creative destruction) is central to classic concepts of macroevolution1,2. However, the relative impacts of extinction and radiation on the co-occurrence of species have not been directly quantitatively compared across the Phanerozoic eon. Here we apply machine learning to generate a spatial embedding (multidimensional ordination) of the temporal co-occurrence structure of the Phanerozoic fossil record, covering 1,273,254 occurrences in the Paleobiology Database for 171,231 embedded species. This facilitates the simultaneous comparison of macroevolutionary disruptions, using measures independent of secular diversity trends. Among the 5% most significant periods of disruption, we identify the ‘big five’ mass extinction events2, seven additional mass extinctions, two combined mass extinction–radiation events and 15 mass radiations. In contrast to narratives that emphasize post-extinction radiations1,3, we find that the proportionally most comparable mass radiations and extinctions (such as the Cambrian explosion and the end-Permian mass extinction) are typically decoupled in time, refuting any direct causal relationship between them. Moreover, in addition to extinctions4, evolutionary radiations themselves cause evolutionary decay (modelled co-occurrence probability and shared fraction of species between times approaching zero), a concept that we describe as destructive creation. A direct test of the time to over-threshold macroevolutionary decay4 (shared fraction of species between two times ≤ 0.1), counted by the decay clock, reveals saw-toothed fluctuations around a Phanerozoic mean of 18.6 million years. As the Quaternary period began at a below-average decay-clock time of 11 million years, modern extinctions further increase life’s decay-clock debt

Sclerite-bearing annelids from the lower Cambrian of South China

Cambrian annelids are strikingly diverse and reveal important details of annelid character acquisition. Their contribution, however, to a wider understanding of the evolution of the trochozoans (encompassing the annelids as well as such groups as the brachiopods and molluscs) remains limited. Thus the early annelids had been linked to a variety of cataphract Cambrian metazoans, notably Wiwaxia and the halkieriids, but recent work assigns such fossils to stem-group molluscs. Here we report two new annelids from the Lower Cambrian Chengjiang Lagerstätte, South China. Ipoliknus avitus n. gen., n. sp. is biramous with neurochaetae and notochaetae, but significantly also bears dorsal spinose sclerites and dorso-lateral dentate sclerites. Adelochaeta sinensis n. gen., n. sp. is unique amongst Cambrian polychaetes in possessing the rod-like supports of the parapodia known as aciculae. This supports phylogenetic placement of Adelochaeta as sister to some more derived aciculate Palaeozoic taxa, but in contrast Ipoliknus is recovered as the most basal of the stem-group annelids. Sclerites and chaetae of I. avitus are interpreted respectively as the remnants and derivatives of a once more extensive cataphract covering that was a characteristic of more primitive trochozoans. The two sets of chaetae (noto- and neurochaetae) and two sets of sclerites (spinose and dentate) suggest that in a pre-annelid an earlier and more complete scleritome may have consisted of four zones of sclerites. Other cataphract taxa from the Lower Palaeozoic show a variety of scleritome configurations but establishing direct links with such basal annelids as Ipoliknus at present must remain conjectural

Deep learning on butterfly phenotypes tests evolution’s oldest mathematical model

Traditional anatomical analyses captured only a fraction of real phenomic information. Here, we apply deep learning to quantify total phenotypic similarity across 2468 butterfly photographs, covering 38 subspecies from the polymorphic mimicry complex of Heliconius erato and Heliconius melpomene. Euclidean phenotypic distances, calculated using a deep convolutional triplet network, demonstrate significant convergence between interspecies co-mimics. This quantitatively validates a key prediction of Müllerian mimicry theory, evolutionary biology’s oldest mathematical model. Phenotypic neighbor-joining trees are significantly correlated with wing pattern gene phylogenies, demonstrating objective, phylogenetically informative phenome capture. Comparative analyses indicate frequency-dependent mutual convergence with coevolutionary exchange of wing pattern features. Therefore, phenotypic analysis supports reciprocal coevolution, predicted by classical mimicry theory but since disputed, and reveals mutual convergence as an intrinsic generator for the unexpected diversity of Müllerian mimicry. This demonstrates that deep learning can generate phenomic spatial embeddings, which enable quantitative tests of evolutionary hypotheses previously only testable subjectively

A possible Cambrian stem-group gnathiferan-chaetognath from the Weeks Formation (Miaolingian) of Utah

In recent years the plethora of “weird wonders”, the vernacular for the apparently extinct major bodyplans documented in many of the Cambrian Lagerstätten, has been dramatically trimmed. This is because various taxa have either been assigned to known phyla or at least accommodated in larger monophyletic assemblages. Nevertheless, a number of Cambrian taxa retain their enigmatic status. To this intriguing roster we add Dakorhachis thambus n. gen. n. sp., from the Miaolingian (Guzhangian) Weeks Formation Konservat-Lagerstätte of Utah. Specimens consist of an elongate body lacking appendages, but which is apparently segmented. A prominent feeding apparatus consists of a circlet of triangular teeth, while posteriorly there are three distinct skeletal components. D. thambus n. sp. is interpreted as an ambush predator and may have been partially infaunal. The wider affinities of this new taxon remain conjectural but it is suggested that it may represent a stem-group member of the Gnathifera, today represented by the gnathostomulids, micrognathozoans, rotifers, and possibly with links also to the chaetognaths

Integrated records of environmental change and evolution challenge the Cambrian Explosion.

The 'Cambrian Explosion' describes the rapid increase in animal diversity and abundance, as manifest in the fossil record, between ~540 and 520 million years ago (Ma). This event, however, is nested within a far more ancient record of macrofossils extending at least into the late Ediacaran at ~571 Ma. The evolutionary events documented during the Ediacaran-Cambrian interval coincide with geochemical evidence for the modernisation of Earth's biogeochemical cycles. Holistic integration of fossil and geochemical records leads us to challenge the notion that the Ediacaran and Cambrian worlds were markedly distinct, and places biotic and environmental change within a longer-term narrative. We propose that the evolution of metazoans may have been facilitated by a series of dynamic and global changes in redox conditions and nutrient supply, which, potentially together with biotic feedbacks, enabled turnover events that sustained multiple phases of radiation. We argue that early metazoan diversification should be recast as a series of successive, transitional radiations that extended from the late Ediacaran and continued through the early Palaeozoic. We conclude that while the Cambrian Explosion represents a radiation of crown-group bilaterians, it was simply one phase amongst several metazoan radiations, some older and some younger

Australian spiny mountain crayfish and their temnocephalan ectosymbionts: an ancient association on the edge of coextinction?

Australian spiny mountain crayfish (Euastacus, Parastacidae) and their ecotosymbiotic temnocephalan flatworms (Temnocephalida, Platyhelminthes) may have co-occurred and interacted through deep time, during a period of major environmental change. Therefore, reconstructing the history of their association is of evolutionary, ecological, and conservation significance. Here, time-calibrated Bayesian phylogenies of Euastacus species and their temnocephalans (Temnohaswellia and Temnosewellia) indicate near-synchronous diversifications from the Cretaceous. Statistically significant cophylogeny correlations between associated clades suggest linked evolutionary histories. However, there is a stronger signal of codivergence and greater host specificity in Temnosewellia, which co-occurs with Euastacus across its range. Phylogeography and analyses of evolutionary distinctiveness (ED) suggest that regional differences in the impact of climate warming and drying had major effects both on crayfish and associated temnocephalans. In particular, Euastacus and Temnosewellia show strong latitudinal gradients in ED and, conversely, in geographical range size, with the most distinctive, northern lineages facing the greatest risk of extinction. Therefore, environmental change has, in some cases, strengthened ecological and evolutionary associations, leaving host-specific temnocephalans vulnerable to coextinction with endangered hosts. Consequently, the extinction of all Euastacus species currently endangered (75%) predicts coextinction of approximately 60% of the studied temnocephalans, with greatest loss of the most evolutionarily distinctive lineages

Phylogenetic Codivergence Supports Coevolution of Mimetic Heliconius Butterflies

The unpalatable and warning-patterned butterflies _Heliconius erato_ and _Heliconius melpomene_ provide the best studied example of mutualistic Müllerian mimicry, thought – but rarely demonstrated – to promote coevolution. Some of the strongest available evidence for coevolution comes from phylogenetic codivergence, the parallel divergence of ecologically associated lineages. Early evolutionary reconstructions suggested codivergence between mimetic populations of _H. erato_ and _H. melpomene_, and this was initially hailed as the most striking known case of coevolution. However, subsequent molecular phylogenetic analyses found discrepancies in phylogenetic branching patterns and timing (topological and temporal incongruence) that argued against codivergence. We present the first explicit cophylogenetic test of codivergence between mimetic populations of _H. erato_ and _H. melpomene_, and re-examine the timing of these radiations. We find statistically significant topological congruence between multilocus coalescent population phylogenies of _H. erato_ and _H. melpomene_, supporting repeated codivergence of mimetic populations. Divergence time estimates, based on a Bayesian coalescent model, suggest that the evolutionary radiations of _H. erato_ and _H. melpomene_ occurred over the same time period, and are compatible with a series of temporally congruent codivergence events. This evidence supports a history of reciprocal coevolution between Müllerian co-mimics characterised by phylogenetic codivergence and parallel phenotypic change

The two phases of the Cambrian Explosion

Abstract The dynamics of how metazoan phyla appeared and evolved – known as the Cambrian Explosion – remains elusive. We present a quantitative analysis of the temporal distribution (based on occurrence data of fossil species sampled in each time interval) of lophotrochozoan skeletal species (n = 430) from the terminal Ediacaran to Cambrian Stage 5 (~545 – ~505 Million years ago (Ma)) of the Siberian Platform, Russia. We use morphological traits to distinguish between stem and crown groups. Possible skeletal stem group lophophorates, brachiopods, and molluscs (n = 354) appear in the terminal Ediacaran (~542 Ma) and diversify during the early Cambrian Terreneuvian and again in Stage 2, but were devastated during the early Cambrian Stage 4 Sinsk extinction event (~513 Ma) never to recover previous diversity. Inferred crown group brachiopod and mollusc species (n = 76) do not appear until the Fortunian, ~537 Ma, radiate in the early Cambrian Stage 3 (~522 Ma), and with minimal loss of diversity at the Sinsk Event, continued to diversify into the Ordovician. The Sinsk Event also removed other probable stem groups, such as archaeocyath sponges. Notably, this diversification starts before, and extends across the Ediacaran/Cambrian boundary and the Basal Cambrian Carbon Isotope Excursion (BACE) interval (~541 to ~540 Ma), ascribed to a possible global perturbation of the carbon cycle. We therefore propose two phases of the Cambrian Explosion separated by the Sinsk extinction event, the first dominated by stem groups of phyla from the late Ediacaran, ~542 Ma, to early Cambrian stage 4, ~513 Ma, and the second marked by radiating bilaterian crown group species of phyla from ~513 Ma and extending to the Ordovician Radiation

Ediacaran survivors in the Cambrian: suspicions, denials and a smoking gun

The relative timing of extinctions and originations is a foundation for reconstructing evolutionary causes. However, there has been a tendency to dismiss reported Ediacaran holdovers in favour of effective extinction around the Cambrian boundary. Here, focussing on the classically-Ediacaran frondose biota (Petalonamae), I suggest four main reasons why proposed Ediacaran survivors have previously been denied the acceptance they deserve: denials based on mistaken identity, doppelgängers, a last gasp or dead clades walking. I then point to the lower Cambrian species Stromatoveris psygmoglena as a key example which simultaneously meets these objections. Collectively, Cambrian survivors are a “smoking gun” showing that extinction of the classically-Ediacaran frondose biota did not occur until at least 33 My after the end of the Ediacaran period, registered by phylogenetic petalonamid Thaumaptilon from the Burgess Shale. Therefore, to paraphrase Mark Twain, reports of their earlier demise have been greatly exaggerated. Causes of their ultimate extinction should instead be sought in their total range and diversity dynamics. Overall, the Ediacaran-Cambrian transition shows extremely low numbers of recorded survivors, but diversity dynamics are dominated by the Cambrian explosion. In this context, recorded occurrences for the classically-Ediacaran frondose biota are compatible with at least two extinction events, the first within a possible mass extinction at the Cambrian boundary, and later, their ultimate extinction in, or after, the middle Cambrian (Miaolingian Series, Wuliuan Stage). There is, however, no correlative basis for a causal link between the Cambrian transition and the effective or final demise of the classically-Ediacaran soft-bodied biota